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Geographic Patterns of Morphological Variation in the Lizard Podarcis Carbonelli, a Species with Fragmented Distribution

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Geographic Patterns of Morphological Variation in the Lizard Podarcis Carbonelli, a Species with Fragmented Distribution HERPETOLOGICAL JOURNAL 20: 41–50, 2010 Geographic patterns of morphological variation in the lizard Podarcis carbonelli, a species with fragmented distribution Antigoni Kaliontzopoulou1,2, Miguel A. Carretero1 & Neftalí Sillero3 1CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Vairão, Portugal 2Departament de Biologia Animal (Vertebrats), Facultat de Biologia, Universitat de Barcelona, Spain 3Centro de Investigação em Ciências Geo-Espaciais (CICGE), Universidade do Porto, Portugal Podarcis carbonelli is a lacertid lizard endemic to the western Iberian Peninsula, with a highly fragmented distribution and complex patterns of phylogeographic structure. Here, we investigate intraspecific morphological variability in this species, considering both biometric and pholidotic traits. Our results reveal local patterns of variation in total body size and scalation, but also indicate the existence of gradual, geographically structured morphological variation when size- independent biometry is considered. Total body size is the main factor determining variation across our sample, but this seems to be the result of within-population variability in this trait and is not geographically structured. The southern isolated populations seem highly differentiated in morphological terms, a pattern that also corresponds to singular environmental conditions and distinctive genetic variation, and should therefore be the focus of special attention for future investigation and conservation. Key words: biometry, scalation, Iberian Peninsula, intraspecific variation INTRODUCTION 1981), P. carbonelli has been shown to constitute a dis- tinct evolutionary entity, with an independent odarcis carbonelli Pérez-Mellado, 1981 is a lacertid phylogenetic history (Harris & Sá-Sousa, 2001, 2002; Plizard displaying a set of eco- and phylogeographic Pinho et al., 2006), and is therefore now treated as a full traits that are unique among the herpetological species of the Iberian Peninsula. Endemic to western Iberia, this spe- cies ranges from the Western Central System in Spain and Portugal (Pérez-Mellado, 1981), through the northern coast of Portugal south of the Douro river southwards along the Portuguese coast, where a progressively nar- rower stripe ends in a line of scattered populations (Sá-Sousa, 1999, 2000, 2001a), and finally, an isolate in Doñana, around the Guadalquivir river mouth in Spain (Sá-Sousa et al., 2001; Harris et al., 2002; Fig. 1). In its ecogeographic affinities, it is associated with Atlantic and sub-Atlantic conditions, with climatic variables such as the number of frost days per year, temperature and pre- cipitation apparently acting as determining factors (Sá-Sousa, 2001a). However, recent studies indicate that such environmental conditions clearly differ among the geographic subranges of the species, when modelled as separate units (Carretero & Sillero, submitted). Based on the peculiar shape of its distribution range, it has been suggested that this species may have previously been more widely distributed and became restricted to its present range due to climatic modifications during the Fig. 1. Map showing the distribution of P. carbonelli in Pleistocene and Holocene (Sá-Sousa, 2001a, 2002). Be- 10 x 10 UTM squares (grey), the location of the study cause of this reduced and fragmented range, P. populations (see Table 1 for details) and the 20 km carbonelli was first considered as vulnerable in Portugal buffer used for interpolation of morphological (Cabral, 2005) and is now classified as endangered by the characters. Notice that this buffer does not represent IUCN (Sá-Sousa et al., 2008). the actual distribution of the species – which is in fact First given a separate taxonomic status as a subspe- much more restricted – but was used in order to be able cies of Podarcis bocagei (Seoane 1884) (Pérez-Mellado, to visualize geographical patterns of variation. Correspondence: Antigoni Kaliontzopoulou, CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, Rua Padre Armando Quintas, 4485-671, Vairão, Portugal. E-mail: [email protected] 41 A. Kaliontzopoulou et al. Table 1. Sample localities, geographic coordinates (in WGS1984), altitude in metres, general habitat characterization, sample sizes for males (Nm) and females (Nf) and mean body size as represented by SVL in males and females (SVLm and SVLf). Geographic Locality coordinates Alt. Habitat Nm Nf SVLm SVLf El Casarito 40°31.39'N, 6°8.41'W 1070 Oak forest 8 9 46.67 49.09 Villasrubias 40°20.29'N, 6°38.42'W 850 Oak forest 7 19 51.88 48.71 Peñaparda 40°19.26'N, 6°40.22'W 890 Oak forest 11 15 49.11 52.26 Navasfrías 40°17.69'N, 6°49.29'W 895 Oak forest 7 9 47.64 51.28 Vale do Rossim 40°24.11'N, 7°35.25'W 1392 Mountain shrubland/ 14 5 54.30 55.11 granite walls Espinho 41°1.65'N, 8°38.73'W 0 Coastal dunes 10 10 51.39 46.93 Torreira 40°45.79'N, 8°42.62'W 0 Coastal dunes 10 10 49.92 47.54 Berlenga isl. 39°24.90'N, 9°30.66'W 75 Granite rocks 10 10 57.07 54.23 Cabo Raso 38°42.56'N, 9°29.12'W 0 Human constructions/ 10 10 48.41 46.82 coastal dunes Monte Clérigo 37°20.39'N, 8°51.23'W 0 Human constructions/ 8 11 45.90 48.31 coastal dunes El Acebuche 37°2.87'N, 6°33.94'W 46 Human constructions/ 9 10 47.62 46.96 coastal dunes species (Sá-Sousa & Harris, 2002). In fact, numerous subspecies (P. c. berlengensis) (Vicente, 1985; Sá-Sousa phylogenetic studies have shown that P. carbonelli is et al., 2000; Harris & Sá-Sousa, 2001). Nevertheless, an ex- not directly related to P. bocagei, but is instead a sister tensive morphological characterization of different taxon to the mitochondrial lineage denominated “P. populations of P. carbonelli is still lacking. hispanica type 2” (Harris & Sá-Sousa, 2002; Pinho et al., Here, we examine biometric and pholidotic variation 2006). Additional analyses of intraspecific genetic vari- among eleven populations of P. carbonelli from across ability have corroborated previous biogeographic the whole distribution range of the species, in order to 1) hypotheses since mtDNA markers show a shallow but investigate patterns of morphological variability, 2) de- evident phylogeographic differentiation, the Doñana iso- tect characters that contribute to intraspecific late being quite divergent (Pinho et al., 2007). On the other morphological patterns and 3) analyse the geographical hand, examination of allozyme and microsatellite markers consistency of such patterns. has revealed the existence of local variation, indicating a complex but recent history of fragmentation and high lev- MATERIALS AND METHODS els of variability remaining in Doñana (Pinho, 2007; Pinho et al., in press). Specimens examined In contrast to detailed investigations of In order to quantify morphological differentiation in P. phylogeographic patterns, little is known of the carbonelli we examined specimens belonging to 11 intraspecific morphological differentiation of P. populations from across the distribution range of the spe- carbonelli. Previous studies have mainly focused on and cies (Fig. 1, Table 1). Some of the specimens were comprehensively documented the morphological differ- captured by noose and examined directly in the field, entiation between this species and P. bocagei while others came from museum collections (see Ac- (Pérez-Mellado, 1981; Pérez-Mellado & Galindo, 1986; Sá- knowledgements for details). Although it has been Sousa, 2001b; Harris & Sá-Sousa, 2001; Sá-Sousa & suggested that preservation may have some influence on Harris, 2002; Kaliontzopoulou et al., 2005), as a result of morphological analyses (Vervust et al., 2009), preliminary the initial taxonomic adscription of both species and their analyses did not indicate a significant effect of this factor overall morphological resemblance when compared to the in our sample (nested ANOVA design controlling for remaining Iberian Podarcis. In such studies, P. preservation, P>0.05 in all cases); we therefore performed carbonelli is only represented by a few populations from subsequent analyses not taking this factor into account. a part of the distribution range. Additionally, the isolate of Doñana was only detected in 2001 (Sá-Sousa et al., Morphological characters quantified 2001) and definitely ascribed to P. carbonelli in 2002 We examined morphological variation taking into account (Harris et al., 2002), and its morphological properties have both biometry and scalation. We measured a total of 10 never been examined. In contrast, various studies have biometric characters to the closest 0.01mm using elec- explored the morphological differentiation of the popula- tronic callipers, including snout–vent length (SVL), trunk tion of Berlenga island, usually treated as a separate length (TRL), head length (HL), head width (HW), head 42 Morphology of Podarcis carbonelli height (HH), forelimb length (FLL), femur length (FL), tibia Table 2. Results of the ANOVAs conducted on length (TBL), hind foot length including the fourth toe biometric and pholidotic variables. df: Degrees of and the nail (4TL) and hind limb length (HLL). All meas- freedom for each effect, F: value of the statistic, P: urements were taken by the same person (AK) to minimize corresponding P-value. Significant P-values (at a=0.05) measurement error. For scalation we quantified five are marked in italics. See Materials and Methods for pholidotic characters including the number of collar variable abbreviations. scales (CSN), gular scales (GSN), transversal rows of ven- tral scales (VSN), femoral pores (FPN) and supratemporal SEX SITE SEX*SITE scales (StSN). For all bilateral characters, both biometric Biometry* df 1 10 10 and pholidotic, we always considered the right side of the SVL F 0.10 8.62 2.43 body. P 0.757 <0.001 0.009 Statistical analyses TRL F 60.93 9.25 2.31 P <0.001 <0.001 0.014 All variables were log-transformed prior to analyses to ensure normality (Lilliefors test, P>0.1) and homogeneity HL F 164.26 9.21 1.75 of variances (Levene’s test, P>0.05).
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